Tetracycline Resistance among Escherichia coli Isolates from Broilers in Iran: A Systematic Review and Meta-Analysis
-
Aliasghar Fakhri-Demeshghieh
,
Hamideh Hasannejad
,
Parniyan Khoramian
,
Vahid Rahmanian
,
Alireza Bahonar
Abstract
Background: Avian colibacillosis are infections caused by Avian Pathogenic Escherichia coli which causes high morbidity, high mortality, and significant economic losses. Antibiotics such as tetracycline are an important treatment choice for colibacillosis in Iran. However, the irrational use of antibiotics has caused high antibiotic resistance. The aim of this study was to estimate the tetracycline resistance rate among E. coli isolates from broilers in Iran.
Methods: PubMed, Scopus, Web of Science, Google Scholar, Islamic World Science Citation, Scientific Information Database, and MagIran databases were searched from 2013 and 2023. Risk of bias assessment was assessed with Appraisal tool for Cross-Sectional Studies. For meta-analysis, a random effects model with Freeman-Tukey double arcsine transformation was used. Subgroup analysis for the year of publication and sensitivity analysis to assess the influence of individual studies were conducted and a province-level map of point estimates was drawn.
Results: Among 13 included studies, the pooled tetracycline resistance was 85% (95% CI: 76-92%) and I-squared was 94.29%. In subgroup analysis, resistance rate was higher for articles published in 2018-2023 (91%) compared to articles published in 2013-2017 (76%), but heterogeneity between groups was not statistically-significant (P=0.12). sensitivity analysis showed that the omission of individual studies caused no apparent change. The province-level map showed that most of the studies belonged to northern parts of Iran with Ardabil (99.65%) having the highest value.
Conclusion: Resistance against tetracycline in E. coli isolates from broilers in Iran is alarming. The sensible use of tetracycline is advised.
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5. Kamil MAIM, Abu-Bakar L, Reduan MFH, et al (2023). The Use of Medicinal Plants in Avian Colibacillosis Management: A Review. Veterinary Integrative Sciences, 21 (2):507-522.
6. Pakbin B, Allahyari S, Amani Z, et al (2021). Prevalence, phylogroups and antimicrobial susceptibility of Escherichia coli isolates from food products. Antibiotics (Basel), 10 (11):1291.
7. Abou-Jaoudeh C, Khalil J, El-Hayek E, et al (2024). Food safety control in poultry industry: prevalence and antimicrobial susceptibility of Escherichia coli isolated from raw chicken and the potential use of Origanum essential oils as alternative to antibiotics. Br Poult Sci, 65(4):494-501.
8. Jaiswal A, Khan A, Yogi A, et al (2024). Isolation and molecular characterization of multidrug‑resistant Escherichia coli from chicken meat. 3 Biotech, 14 (4):107.
9. Jahantigh M, Samadi K, Dizaji RE, Salari S (2020). Antimicrobial resistance and prevalence of tetracycline resistance genes in Escherichia coli isolated from lesions of colibacillosis in broiler chickens in Sistan, Iran. BMC Vet Res, 16 (1):267.
10. Gholami-Ahangaran M, Karimi-Dehkordi M, Miranzadeh-Mahabadi E, et al (2021). The frequency of tetracycline resistance genes in Escherichia coli strains isolated from healthy and diarrheic pet birds. Iran J Vet Res, 22 (4):337-341.
11. Azizpour A (2022). Determination of antibiotic resistance patterns of Escherichia coli strains to twenty antibiotics used in the Iran. Journal of Sabzevar University of Medical Sciences, 29 (1):101-114.
12. Pourhossein Z, Asadpour L, Habibollahi H, et al (2022). Antibacterial Resistance and Virulence Potential of Avian Colibacillosis-Causing Escherichia coli Isolates. Infection Epidemiology and Microbiology, 8 (4):307-315.
13. Page MJ, McKenzie JE, Bossuyt PM, et al (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Int J Surg, 88:105906.
14. Downes MJ, Brennan ML, Williams HC, et al (2016). Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open, 6 (12):e011458.
15. Palma E, Tilocca B, Roncada P (2020). Antimicrobial resistance in veterinary medicine: An overview. Int J Mol Sci, 21 (6):1914.
16. Sjoberg AM, Fellman CL, DeStefano IM, et al (2023). One Health interprofessional stewardship to combat antimicrobial resistance. Nat Med, 29(3):512-513.
17. McCormick BP, Quiroga MP, Álvarez VE, et al (2023). Antimicrobial resistance dissemination associated with intensive animal production practices in Argentina: A systematic review and meta-analysis. Rev Argent Microbiol, 55(1):25-42.
18. Pattanayak DS, Pal D, Mishra J, et al (2023). Doped graphitic carbon nitride (g-C3N4) catalysts for efficient photodegradation of tetracycline antibiotics in aquatic environments. Environ Sci Pollut Res, 30 (10):24919-24926.
19. Mulchandani R, Wang Y, Gilbert M, et al (2023). Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Glob Public Health, 3 (2):e0001305.
20. Goudarztalejerdi A, Mohammadzadeh A, Niazi K, et al (2022). High prevalence of multidrug resistance and biofilm-formation ability among avian Escherichia coli isolated from broilers in Iran. Microb Drug Resist, 28 (2):244-254.
21. Adabi M, Reza Faryabi M, Nili-Ahmadabadi A, et al (2022). Evaluation of tetracycline antibiotics residues in chicken tissues using the four-plate test, ELISA, and HPLC methods in Iran. International Journal of Environmental Analytical Chemistry, 104(3):1-10.
22. Sebastian S, Tom AA, Babu JA, et al (2021). Antibiotic resistance in Escherichia coli isolates from poultry environment and UTI patients in Kerala, India: A comparison study. Comp Immunol Microbiol Infect Dis, 75:101614.
23. Islam M, Hossain M, Sobur M, et al (2023). A Systematic Review on the Occurrence of Antimicrobial-Resistant Escherichia coli in Poultry and Poultry Environments in Bangladesh between 2010 and 2021. Biomed Res Int, 2023: 2425564.
24. Andre PB, Wilfried D, Abiezer DR, et al (2021). Antibiotic resistance in food producing Animals in West Africa French speaking countries: A systematic review. African Journal of Microbiology Research, 15 (1):47-61.
25. Phu DH, Wongtawan T, Truong DB, et al (2022). A systematic review and meta-analysis of integrated studies on antimicrobial resistance in Vietnam, with a focus on Enterobacteriaceae, from a One Health perspective. One Health, 15:100465.
26. Alsayeqh AF, Baz AHA, Darwish WS (2021). Antimicrobial-resistant foodborne pathogens in the Middle East: A systematic review. Environ Sci Pollut Res Int, 28 (48):68111-68133.
27. Mesa-Varona O, Kaspar H, Grobbel M, et al (2020). Phenotypical antimicrobial resistance data of clinical and non-clinical Escherichia coli from poultry in Germany between 2014 and 2017. PLoS One, 15 (12):e0243772.
28. Willis C, Jørgensen F, Cawthraw S, et al (2023). A survey of Salmonella, Escherichia coli and antimicrobial resistance in frozen, part-cooked, breaded or battered chicken products on retail sale in the United Kingdom. J Appl Microbiol, 134(5):lxad093.
29. Rahimi M (2013). Antibioresistance profile of avian pathogenic Escherichia coli isolates recovered from broiler chicken farms with colibacillosis in Kermanshah province, Iran. Global Veterinaria, 10 (4):447-452.
30. Kazemnia A, Ahmadi M, Dilmaghani M (2014). Antibiotic resistance pattern of different Escherichia coli phylogenetic groups isolated from human urinary tract infection and avian colibacillosis. Iran Biomed J, 18 (4):219-24.
31. Seifi S, Khoshbakht R, Atabak A (2015). Antibiotic susceptibility, serotyping and pathogenicity evaluation of avian Escherichia coli isolated from broilers in northern Iran. Bulgarian Journal of Veterinary Medicine, 18 (2): 173-179.
32. Seifi S, Khoshbakht R (2016). Prevalence of tetracycline resistance determinants in broiler isolated Escherichia coli in Iran. Br Poult Sci, 57 (6):729-733.
33. Kheiri R, Ranjbar R, Khamesipour F, et al (2016). Role of antibiotic in drug resistance and integrons prevalence in Escherichia coli isolated from human and animal specimens. Kafkas Univ Vet Fak Derg, 22(6): 953–959.
34. Azizpour A, Saeidi Namin V (2017). Investigation of antibiotic resistance patterns in Escherichia coli isolated from broiler chickens with colibacillosis to ten antibacterial agents commonly used in the Iranian poultry industry. Journal of Comparative Pathobiology, 14 (4):2345-2352.
35. Asadi A, Zahraei Salehi T, Jamshidiyan M (2018). Molecular analysis of antibiotic resistance genes in Escherichia coli from broiler chickens in shahrebabak by Multiplex PCR Technique. Iranian Journal of Animal Science, 49 (2):203-211.
36. Mohammadi V, Ghaniei A, Sepehrnia P (2018). Antimicrobial resistance profile and prevalence of tetracycline resistance genes in Escherichia coli isolates from broiler chickens, Northwestern Iran. Bulgarian J Vet Med, 21 (2):169-175.
37. Esmaeelzadeh Dizaji R, Jahantigh M, Rashki A (2020). The molecular survey of intI gene and antibacterial resistant in avian pathogenic Escherichia coil. Veterinary Research & Biological Products, 33 (2):68-74.
38. Rezatofighi SE, Najafifar A, Askari Badouei M, et al (2021). An integrated perspective on virulence-associated genes (VAGs), antimicrobial resistance (AMR), and phylogenetic clusters of pathogenic and non-pathogenic avian Escherichia coli. Front Vet Sci, 8:758124.
39. Kalantari M, Sharifiyazdi H, Asasi K, et al (2021). High incidence of multidrug resistance and class 1 and 2 integrons in Escherichia coli isolated from broiler chickens in South of Iran. Vet Res Forum, 12(1):101-107.
2. Ramatla T, Tawana M, Lekota KE, et al (2023). Antimicrobial resistance genes of Escherichia coli, a bacterium of “One Health” importance in South Africa: Systematic review and meta-analysis. AIMS Microbiology, 9 (1):75-89.
3. Mandal AK, Talukder S, Hasan MM, et al (2022). Epidemiology and antimicrobial resistance of Escherichia coli in broiler chickens, farmworkers, and farm sewage in Bangladesh. Vet Med Sci, 8 (1):187-199.
4. Alam GS, Hassan MM, Ahaduzzaman M, et al (2023). Molecular Detection of Tetracycline-Resistant Genes in Multi-Drug-Resistant Escherichia coli Isolated from Broiler Meat in Bangladesh. Antibiotics (Basel), 12 (2):418.
5. Kamil MAIM, Abu-Bakar L, Reduan MFH, et al (2023). The Use of Medicinal Plants in Avian Colibacillosis Management: A Review. Veterinary Integrative Sciences, 21 (2):507-522.
6. Pakbin B, Allahyari S, Amani Z, et al (2021). Prevalence, phylogroups and antimicrobial susceptibility of Escherichia coli isolates from food products. Antibiotics (Basel), 10 (11):1291.
7. Abou-Jaoudeh C, Khalil J, El-Hayek E, et al (2024). Food safety control in poultry industry: prevalence and antimicrobial susceptibility of Escherichia coli isolated from raw chicken and the potential use of Origanum essential oils as alternative to antibiotics. Br Poult Sci, 65(4):494-501.
8. Jaiswal A, Khan A, Yogi A, et al (2024). Isolation and molecular characterization of multidrug‑resistant Escherichia coli from chicken meat. 3 Biotech, 14 (4):107.
9. Jahantigh M, Samadi K, Dizaji RE, Salari S (2020). Antimicrobial resistance and prevalence of tetracycline resistance genes in Escherichia coli isolated from lesions of colibacillosis in broiler chickens in Sistan, Iran. BMC Vet Res, 16 (1):267.
10. Gholami-Ahangaran M, Karimi-Dehkordi M, Miranzadeh-Mahabadi E, et al (2021). The frequency of tetracycline resistance genes in Escherichia coli strains isolated from healthy and diarrheic pet birds. Iran J Vet Res, 22 (4):337-341.
11. Azizpour A (2022). Determination of antibiotic resistance patterns of Escherichia coli strains to twenty antibiotics used in the Iran. Journal of Sabzevar University of Medical Sciences, 29 (1):101-114.
12. Pourhossein Z, Asadpour L, Habibollahi H, et al (2022). Antibacterial Resistance and Virulence Potential of Avian Colibacillosis-Causing Escherichia coli Isolates. Infection Epidemiology and Microbiology, 8 (4):307-315.
13. Page MJ, McKenzie JE, Bossuyt PM, et al (2021). The PRISMA 2020 statement: An updated guideline for reporting systematic reviews. Int J Surg, 88:105906.
14. Downes MJ, Brennan ML, Williams HC, et al (2016). Development of a critical appraisal tool to assess the quality of cross-sectional studies (AXIS). BMJ Open, 6 (12):e011458.
15. Palma E, Tilocca B, Roncada P (2020). Antimicrobial resistance in veterinary medicine: An overview. Int J Mol Sci, 21 (6):1914.
16. Sjoberg AM, Fellman CL, DeStefano IM, et al (2023). One Health interprofessional stewardship to combat antimicrobial resistance. Nat Med, 29(3):512-513.
17. McCormick BP, Quiroga MP, Álvarez VE, et al (2023). Antimicrobial resistance dissemination associated with intensive animal production practices in Argentina: A systematic review and meta-analysis. Rev Argent Microbiol, 55(1):25-42.
18. Pattanayak DS, Pal D, Mishra J, et al (2023). Doped graphitic carbon nitride (g-C3N4) catalysts for efficient photodegradation of tetracycline antibiotics in aquatic environments. Environ Sci Pollut Res, 30 (10):24919-24926.
19. Mulchandani R, Wang Y, Gilbert M, et al (2023). Global trends in antimicrobial use in food-producing animals: 2020 to 2030. PLOS Glob Public Health, 3 (2):e0001305.
20. Goudarztalejerdi A, Mohammadzadeh A, Niazi K, et al (2022). High prevalence of multidrug resistance and biofilm-formation ability among avian Escherichia coli isolated from broilers in Iran. Microb Drug Resist, 28 (2):244-254.
21. Adabi M, Reza Faryabi M, Nili-Ahmadabadi A, et al (2022). Evaluation of tetracycline antibiotics residues in chicken tissues using the four-plate test, ELISA, and HPLC methods in Iran. International Journal of Environmental Analytical Chemistry, 104(3):1-10.
22. Sebastian S, Tom AA, Babu JA, et al (2021). Antibiotic resistance in Escherichia coli isolates from poultry environment and UTI patients in Kerala, India: A comparison study. Comp Immunol Microbiol Infect Dis, 75:101614.
23. Islam M, Hossain M, Sobur M, et al (2023). A Systematic Review on the Occurrence of Antimicrobial-Resistant Escherichia coli in Poultry and Poultry Environments in Bangladesh between 2010 and 2021. Biomed Res Int, 2023: 2425564.
24. Andre PB, Wilfried D, Abiezer DR, et al (2021). Antibiotic resistance in food producing Animals in West Africa French speaking countries: A systematic review. African Journal of Microbiology Research, 15 (1):47-61.
25. Phu DH, Wongtawan T, Truong DB, et al (2022). A systematic review and meta-analysis of integrated studies on antimicrobial resistance in Vietnam, with a focus on Enterobacteriaceae, from a One Health perspective. One Health, 15:100465.
26. Alsayeqh AF, Baz AHA, Darwish WS (2021). Antimicrobial-resistant foodborne pathogens in the Middle East: A systematic review. Environ Sci Pollut Res Int, 28 (48):68111-68133.
27. Mesa-Varona O, Kaspar H, Grobbel M, et al (2020). Phenotypical antimicrobial resistance data of clinical and non-clinical Escherichia coli from poultry in Germany between 2014 and 2017. PLoS One, 15 (12):e0243772.
28. Willis C, Jørgensen F, Cawthraw S, et al (2023). A survey of Salmonella, Escherichia coli and antimicrobial resistance in frozen, part-cooked, breaded or battered chicken products on retail sale in the United Kingdom. J Appl Microbiol, 134(5):lxad093.
29. Rahimi M (2013). Antibioresistance profile of avian pathogenic Escherichia coli isolates recovered from broiler chicken farms with colibacillosis in Kermanshah province, Iran. Global Veterinaria, 10 (4):447-452.
30. Kazemnia A, Ahmadi M, Dilmaghani M (2014). Antibiotic resistance pattern of different Escherichia coli phylogenetic groups isolated from human urinary tract infection and avian colibacillosis. Iran Biomed J, 18 (4):219-24.
31. Seifi S, Khoshbakht R, Atabak A (2015). Antibiotic susceptibility, serotyping and pathogenicity evaluation of avian Escherichia coli isolated from broilers in northern Iran. Bulgarian Journal of Veterinary Medicine, 18 (2): 173-179.
32. Seifi S, Khoshbakht R (2016). Prevalence of tetracycline resistance determinants in broiler isolated Escherichia coli in Iran. Br Poult Sci, 57 (6):729-733.
33. Kheiri R, Ranjbar R, Khamesipour F, et al (2016). Role of antibiotic in drug resistance and integrons prevalence in Escherichia coli isolated from human and animal specimens. Kafkas Univ Vet Fak Derg, 22(6): 953–959.
34. Azizpour A, Saeidi Namin V (2017). Investigation of antibiotic resistance patterns in Escherichia coli isolated from broiler chickens with colibacillosis to ten antibacterial agents commonly used in the Iranian poultry industry. Journal of Comparative Pathobiology, 14 (4):2345-2352.
35. Asadi A, Zahraei Salehi T, Jamshidiyan M (2018). Molecular analysis of antibiotic resistance genes in Escherichia coli from broiler chickens in shahrebabak by Multiplex PCR Technique. Iranian Journal of Animal Science, 49 (2):203-211.
36. Mohammadi V, Ghaniei A, Sepehrnia P (2018). Antimicrobial resistance profile and prevalence of tetracycline resistance genes in Escherichia coli isolates from broiler chickens, Northwestern Iran. Bulgarian J Vet Med, 21 (2):169-175.
37. Esmaeelzadeh Dizaji R, Jahantigh M, Rashki A (2020). The molecular survey of intI gene and antibacterial resistant in avian pathogenic Escherichia coil. Veterinary Research & Biological Products, 33 (2):68-74.
38. Rezatofighi SE, Najafifar A, Askari Badouei M, et al (2021). An integrated perspective on virulence-associated genes (VAGs), antimicrobial resistance (AMR), and phylogenetic clusters of pathogenic and non-pathogenic avian Escherichia coli. Front Vet Sci, 8:758124.
39. Kalantari M, Sharifiyazdi H, Asasi K, et al (2021). High incidence of multidrug resistance and class 1 and 2 integrons in Escherichia coli isolated from broiler chickens in South of Iran. Vet Res Forum, 12(1):101-107.
| Files | ||
| Issue | Vol 54 No 1 (2025) | |
| Section | Review Article(s) | |
| Keywords | ||
| Antimicrobial resistance Escherichia coli Broiler Iran | ||
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How to Cite
1.
Fakhri-Demeshghieh A, Hasannejad H, Khoramian P, Rahmanian V, Bahonar A. Tetracycline Resistance among Escherichia coli Isolates from Broilers in Iran: A Systematic Review and Meta-Analysis. Iran J Public Health. 2025;54(1):101-111.
